The sessile nature of plants subjects them to a constant exposure of biotic and abiotic stresses. Although plants do not have specialized immune cells, they can mount local and systemic immune responses, which require extensive crosstalk between plant defense and other physiological processes [1]. Induction of local defense responses involves recognition of microbe-associated molecular patterns (MAMPs) by membrane-associated receptors, leading to MAMP-triggered immunity (MTI), and recognition of pathogen-delivered effectors by cytosolic receptors, resulting in effector-triggered immunity (ETI) [2]. Salicylic acid (SA) that is produced during local infection events can lead to systemic acquired resistance (SAR). In Arabidopsis, SA signals through a key immune regulator, designated NPR1 (Non-expressor of PR genes), which is involved in regulating changes at the transcriptional level of as many as ˜10% of all genes [3]. Systemic acquired resistance is broad-spectrum and long lasting, compared to the signal-specific MAMP- and effector-triggered immunity responses [4].
SAR-associated transcriptional reprogramming re-directs cellular resources, normally dedicated to growth-related activities, towards de novo synthesis of anti-microbial proteins, such as the pathogenesis-related (PR) proteins. Before PR proteins can accumulate, endoplasmic reticulum (ER)-resident genes encoding the secretory pathway components are coordinately up-regulated to ensure efficient post-translational modification and secretion of the antimicrobial PR peptides [3, 5]. The enhancement of ER components is not restricted to SAR, however, as ER-resident genes have been shown to be involved in MTI. In studies directed to the biogenesis of EFR, a membrane-bound receptor for the MAMP signal elf18 (the N terminal 18 amino acids of the bacterial translation elongation factor Tu, EF-Tu), TBF1 was found to regulate glycosylation pathway genes, including calreticulin 3 (CRT3), and UDP-glucose:glycoprotein glycosyltransferase, STT3A, involved in the ER quality control mechanism (ERQC) required for EFR function [6, 7].
In earlier studies, we demonstrated that induction of both PR and ER-resident genes requires NPR1, a transcription cofactor. Upon induction by SA, NPR1 is translocated to the nucleus [8] inducing PR genes through its interaction with TGA transcription factors (TFs) at the promoters of PR genes [9, 10]. It is not known how NPR1 regulates the ER-resident genes. TGA TFs are not likely candidates, because expression of ER-resident genes is unaltered following induction in tga mutants [3]. Significant enrichment of a novel cis-element TL1 (translocon 1; GAAGAAGAA) in the promoter regions of these NPR1-dependent ER-resident genes suggests the involvement of an unknown TF [3]. Point mutations in the TL1 elements in the BiP2 (Lumenal Binding Protein 2) promoter abolished the inducibility of this gene upon SA treatment, supporting this hypothesis [3]. Identification of the TL1-binding TF is important to our understanding of the mechanism controlling the transition from growth- to defense-responses, as the secretory pathway is required for a wide variety of other cellular functions.
In this study, we report the identification of a heat shock factor-like protein (HSF4/HsfB1) that binds to the TL1 cis-element, which transcriptionally-regulates the expression of genes containing this motif in their promoter regions. We renamed it TL1-Binding Transcription Factor 1, TBF1, since mutants of this transcription factor have normal heat shock responses, but are compromised in the growth-to-defense transition upon challenge by pathogens. The translation of TBF1 is also tightly-regulated through two upstream open reading frames (uORFs) enriched in aromatic amino acids, which are precursors of a large array of plant secondary metabolites involved in defense. Taken together, these observations suggest that TBF1 plays a key role in the general control of events at the transcriptional level in plants.